Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Modulation of spike timing by sensory deprivation during induction of cortical map plasticity

Nature Neuroscience volume 7, pages 534–541 (2004)Cite this article

Abstract

Deprivation-induced plasticity of sensory cortical maps involves long-term potentiation (LTP) and depression (LTD) of cortical synapses, but how sensory deprivation triggers LTP and LTD in vivo is unknown. Here we tested whether spike timing–dependent forms of LTP and LTD are involved in this process. We measured spike trains from neurons in layer 4 (L4) and layers 2 and 3 (L2/3) of rat somatosensory cortex before and after acute whisker deprivation, a manipulation that induces whisker map plasticity involving LTD at L4-to-L2/3 (L4–L2/3) synapses. Whisker deprivation caused an immediate reversal of firing order for most L4 and L2/3 neurons and a substantial decorrelation of spike trains, changes known to drive timing-dependent LTD at L4–L2/3 synapses in vitro. In contrast, spike rate changed only modestly. Thus, whisker deprivation is likely to drive map plasticity by spike timing–dependent mechanisms.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Principal whisker deprivation reduces mean firing rates in behaving rats.
Figure 2: Spike trains elicited by multiwhisker stimulation in L4 and L2/3 of a single S1 column.
Figure 3: Reversal of firing order by principal whisker deprivation for a representative L4–L2 cell pair.
Figure 4: Shift toward synchronized firing by principal whisker deprivation for a representative L4–L3 cell pair.
Figure 5: Effect on mean spike timing across all cell pairs.
Figure 6: Decorrelation of L4 and L2/3 spike trains by principal whisker deprivation.
Figure 7: Quantitative model of STDP from spike timing data measured in vivo.

Similar content being viewed by others

References

  1. Wiesel, T.N. The postnatal development of the visual cortex and the influence of environment. Nature 299, 583–591 (1982).

    Article  CAS  Google Scholar 

  2. Buonomano, D.V. & Merzenich, M.M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149–186 (1998).

    Article  CAS  Google Scholar 

  3. Hebb, D.O. The Organization of Behavior (Wiley, New York, 1949).

    Google Scholar 

  4. Bear, M.F. A synaptic basis for memory storage in the cerebral cortex. Proc. Natl. Acad. Sci. USA 93, 13453–13459 (1996).

    Article  CAS  Google Scholar 

  5. Fregnac, Y. & Shulz, D.E. Activity-dependent regulation of receptive field properties of cat area 17 by supervised Hebbian learning. J. Neurobiol. 41, 69–82 (1999).

    Article  CAS  Google Scholar 

  6. Rioult-Pedotti, M.S., Friedman, D. & Donoghue, J.P. Learning-induced LTP in neocortex. Science 290, 533–536 (2000).

    Article  CAS  Google Scholar 

  7. Allen, C.B., Celikel, T. & Feldman, D.E. Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nat. Neurosci. 6, 291–299 (2003).

    Article  CAS  Google Scholar 

  8. Heynen, A.J. et al. Molecular mechanisms for loss of visual cortical responsiveness following brief monocular deprivation. Nat. Neurosci. 6, 854–862 (2003).

    Article  CAS  Google Scholar 

  9. Finnerty, G.T., Roberts, L.S. & Connors, B.W. Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400, 367–371 (1999).

    Article  CAS  Google Scholar 

  10. Bliss, T.V. & Collingridge, G.L. A synaptic model of memory: long-term potentiation in hippocampus. Nature 361, 31–39 (1993).

    Article  CAS  Google Scholar 

  11. Bear, M.F. & Abraham, W.C. Long-term depression in hippocampus. Annu. Rev. Neurosci. 19, 437–462 (1996).

    Article  CAS  Google Scholar 

  12. Abbott, L.F. & Nelson, S.B. Synaptic plasticity: taming the beast. Nat. Neurosci. 3(Suppl.), 1178–1183 (2000).

    Article  CAS  Google Scholar 

  13. Bi, G. & Poo, M. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu. Rev. Neurosci. 24, 139–166 (2001).

    Article  CAS  Google Scholar 

  14. Sjostrom, P.J., Turrigiano, G.G. & Nelson, S.B. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149–1164 (2001).

    Article  CAS  Google Scholar 

  15. Huber, K.M., Sawtell, N.B. & Bear, M.F. Brain-derived neurotrophic factor alters the synaptic modification threshold in visual cortex. Neuropharmacology 37, 571–579 (1998).

    Article  CAS  Google Scholar 

  16. Dudek, S.M. & Bear, M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl. Acad. Sci. USA 89, 4363–4367 (1992).

    Article  CAS  Google Scholar 

  17. Feldman, D.E. Timing based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27, 45–56 (2000).

    Article  CAS  Google Scholar 

  18. Castro-Alamancos, M.A., Donoghue, J.P. & Connors, B.W. Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex. J. Neurosci. 15, 5324–5333 (1995).

    Article  CAS  Google Scholar 

  19. Bienenstock, E.L., Cooper, L.N. & Munro, P.W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2, 32–48 (1982).

    Article  CAS  Google Scholar 

  20. Song, S., Miller, K.D. & Abbott, L.F. Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat. Neurosci. 3, 919–926 (2000).

    Article  CAS  Google Scholar 

  21. Song, S. & Abbott, L.F. Cortical development and remapping through spike timing-dependent plasticity. Neuron 32, 339–350 (2001).

    Article  CAS  Google Scholar 

  22. Simons, D.J. & Woolsey, T.A. Functional organization in mouse barrel cortex. Brain Res. 165, 327–332 (1979).

    Article  CAS  Google Scholar 

  23. Armstrong-James, M. & Fox, K. Spatiotemporal convergence and divergence in the rat S1 “barrel” cortex. J. Comp. Neurol. 263, 265–281 (1987).

    Article  CAS  Google Scholar 

  24. Glazewski, S. & Fox, K. Time course of experience-dependent synaptic potentiation and depression in barrel cortex of adolescent rats. J. Neurophysiol. 95, 1714–1729 (1996).

    Article  Google Scholar 

  25. Wallace, H., Glazewski, S., Liming, K. & Fox, K. The role of cortical activity in experience-dependent potentiation and depression of sensory responses in rat barrel cortex. J. Neurosci. 21, 3881–3894 (2001).

    Article  CAS  Google Scholar 

  26. Glazewski, S., McKenna, M., Jacquin, M. & Fox, K. Experience-dependent depression of vibrissae responses in adolescent rat barrel cortex. Eur. J. Neurosci. 10, 2107–2116 (1998).

    Article  CAS  Google Scholar 

  27. Margrie, T.W., Brecht, M. & Sakmann, B. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflügers Arch. 444, 491–498 (2002).

    Article  CAS  Google Scholar 

  28. Petersen, C.C., Hahn, T.T., Mehta, M., Grinvald, A. & Sakmann, B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl. Acad. Sci. USA 100, 13638–13643 (2003).

    Article  CAS  Google Scholar 

  29. DeWeese, M.R., Wehr, M. & Zador, A.M. Binary spiking in auditory cortex. J. Neurosci. 23, 7940–7949 (2003).

    Article  CAS  Google Scholar 

  30. deCharms, R.C. & Zador, A. Neural representation and the cortical code. Annu. Rev. Neurosci. 23, 613–647 (2000).

    Article  CAS  Google Scholar 

  31. Vinje, W.E. & Gallant, J.L. Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287, 1273–1276 (2000).

    Article  CAS  Google Scholar 

  32. Kelly, M.K., Carvell, G.E., Kodger, J.M. & Simons, D.J. Sensory loss by selected whisker removal produces immediate disinhibition in the somatosensory cortex of behaving rats. J. Neurosci. 19, 9117–9125 (1999).

    Article  CAS  Google Scholar 

  33. Simons, D.J. Response properties of vibrissa units in rat S1 somatosensory neocortex. J. Neurophysiol. 41, 798–820 (1978).

    Article  CAS  Google Scholar 

  34. Armstrong-James, M., Fox, K. & Das-Gupta, A. Flow of excitation within rat barrel cortex on striking a single vibrissa. J. Neurophysiol. 68, 1345–1358 (1992).

    Article  CAS  Google Scholar 

  35. Gerstein, G.L. Correlation-based analysis methods for neural ensemble data. in Methods for Ensemble Recordings (ed. Nicolelis, M.A.L.) 158–178 (CRC Press, New York, 1999).

    Google Scholar 

  36. Tsodyks, M., Kenet, T., Grinvald, A. & Arieli, A. Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286, 1943–1946 (1999).

    Article  CAS  Google Scholar 

  37. Zhang, L.I., Tao, H.W., Holt, C.E., Harris, W.A. & Poo, M.A. critical window for cooperation and competition among developing retinotectal synapses. Nature 395, 37–44 (1998).

    Article  CAS  Google Scholar 

  38. Froemke, R.C. & Dan, Y. Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416, 433–438 (2002).

    Article  CAS  Google Scholar 

  39. Yao, H. & Dan, Y. Stimulus timing-dependent plasticity in cortical processing of orientation. Neuron 32, 315–323 (2001).

    Article  CAS  Google Scholar 

  40. Fu, Y.X. et al. Temporal specificity in the cortical plasticity of visual space representation. Science 296, 1999–2003 (2002).

    Article  CAS  Google Scholar 

  41. Goldreich, D., Kyriazi, H.T. & Simons, D.J. Functional independence of layer IV barrels in rodent somatosensory cortex. J. Neurophysiol. 82, 1311–1316 (1999).

    Article  CAS  Google Scholar 

  42. Petersen, C.C. & Sakmann, B. The excitatory neuronal network of rat layer 4 barrel cortex. J. Neurosci. 20, 7579–7586 (2000).

    Article  CAS  Google Scholar 

  43. Schubert, D., Kotter, R., Zilles, K., Luhmann, H.J. & Staiger, J.F. Cell-type specific circuits of cortical layer IV spiny neurons. J. Neurosci. 23, 2961–2970 (2003).

    Article  CAS  Google Scholar 

  44. Trachtenberg, J.T., Trepel, C. & Stryker, M.P. Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. Science 287, 2029–2032 (2000).

    Article  CAS  Google Scholar 

  45. Panzeri, S., Petersen, R.S., Schultz, S.R., Lebedev, M. & Diamond, M.E. The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29, 769–777 (2001).

    Article  CAS  Google Scholar 

  46. Paulsen, O. & Sejnowski, T.J. Natural patterns of activity and long-term synaptic plasticity. Curr. Opin. Neurobiol. 10, 172–179 (2000).

    Article  CAS  Google Scholar 

  47. Singer, W. & Gray, C.M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995).

    Article  CAS  Google Scholar 

  48. Fee, M.S., Mitra, P.P. & Kleinfeld, D. Automatic sorting of multiple unit neuronal signals in the presence of anisotropic and non-Gaussian variability. J. Neurosci. Methods 69, 175–188 (1996).

    Article  CAS  Google Scholar 

  49. Fanselow, E.E. & Nicolelis, M.A.L. Behavioral modulation of tactile responses in the rat somatosensory cortex. J. Neurosci. 19, 7603–7616 (1999).

    Article  CAS  Google Scholar 

  50. Brumberg, J.C., Pinto, D.J. & Simons, D.J. Cortical columnar processing in the rat whisker-to-barrel system. J. Neurophysiol. 82, 1808–1817 (1999).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. Rangel, S. Pahlavan and G. Wong for behavioral analysis, and D. Kleinfeld and S. Mehta for spike sorting software. We are grateful to B. Kristan, P. Reinagel, M. Feller and Feldman lab members for reading the manuscript. Recording arrays were provided by University of Michigan Center for Neural Communication Technology (supported by National Institutes of Health grant NCRR P41-RR09754). This work was supported by March of Dimes (5-FY01-485) and National Institute of Neurological Disorders and Stroke (1 R01 NS046652). D.E.F. is an Alfred P. Sloan Research Fellow.

Author information

Author notes

  1. Tansu Celikel

    Present address: Department of Cell Physiology, Max-Planck Institute for Medical Research, Jahnstrasse 29, Heidelberg, D-69120, Germany

Authors and Affiliations

  1. Division of Biological Sciences, University of California San Diego, 9500 Gilman Drive, La Jolla, 92093, California, USA

    Tansu Celikel, Vanessa A Szostak & Daniel E Feldman

Authors
  1. Tansu Celikel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vanessa A Szostak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniel E Feldman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel E Feldman.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Reduction in whisker-evoked spike count following PW cut. Response strength (spike per stimulus) for each stimulus condition. Following PW cut, response strength was reduced significantly in L4 (n = 40 units) and L3 (n = 23 units), but not in L2 (n = 21 units). Asterisks, P < 0.05 (unpaired 2-tailed t-test). (GIF 7 kb)

Supplementary Fig. 2

Controls for stationarity of spike trains. (a) Long-duration recordings (4200 sweeps [700 ms sweep duration] over ~75 minutes) for four simultaneously recorded L4-L2 cell pairs during spontaneous firing (left), and multiwhisker-evoked firing (right). (b) Response latency, whisker-evoked spike count (spikes/stimulus), and CCG peak were stationary over 45 minutes (the duration of the standard recording protocol). Inset at right, distribution of changes in CCG peaks for all pairs between 15 and 45 minutes. (c) Response latency, whisker-evoked spike count, and CCG peak before and advancement of the whisker deflection mesh 1 mm towards face without cutting the PW ("Sham cut"). (This was the procedure used to assess recovery from PW cut in the main experiments). Sham cut and mesh advancement produced no significant changes in any of these measures. Inset at right, distribution of changes in CCG peaks for all pairs before and after sham cut. (GIF 30 kb)

Supplementary Fig. 3

Acute alterations in firing patterns by PW cut. (a) Mean normalized PSTHs across all units for multiwhisker response (black traces) and after PW cut (gray traces). Pspike is the probability of observing a spike in each 1 ms time bin. PW cut caused latency to increase in L4 and L3, but to decrease in L2 (see Table 1). These changes in response latency explain the spike timing changes observed in L4-L2 and L4-L3 cell pairs (see text). (b) Mean normalized ISI distributions for all units. PW cut altered the ISI distribution for L4 (P < 0.05, Kolmogorov-Smirnov test), but not L2 or L3 (P > 0.1). (c) Mean distribution of spikes per stimulus (response strength) for all units, calculated from a 50 ms time window after whisker deflection. PW cut did not significantly alter the distribution of response strength for any layer (P > 0.05, t-test). (GIF 15 kb)

Supplementary Methods (PDF 10 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Celikel, T., Szostak, V. & Feldman, D. Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat Neurosci 7, 534–541 (2004). https://doi.org/10.1038/nn1222

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1222

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing